This volume concerns the current global extinction crisis for amphibians and the coordinated response of zoos and aquariums around the world, and it is the first International Zoo Yearbook devoted in large part to amphibians [but see IZY Volume 9 (1969), Volume 19 (1979) and Volume 28 (1989)]. These zoological institutions – along with important partners in the governmental, museum, university, botanical garden and private sector – have the collective experience, capabilities, networks, facilities and other resources to tackle this crisis in a meaningful and systematic way. The research, husbandry, educational, awareness raising, publicity and other vital activities reported on here take place under the aegis of an ‘Amphibian Ark’– a unique partnership initiative between the World Association of Zoos and Aquariums, the IUCN/SSC Amphibian Specialist Group and the IUCN/SSC Conservation Breeding Specialist Group (see Pavajeau et al., in press).
The general concept of an ‘Ark’ needs to be set in the context of the evolution of the function of zoos and aquariums in the mid-to-late 20th century. During this period, partly in response to public criticism, zoos and aquariums of the world laid major claim to an area of conservation where no other agencies operated to any great extent. ‘Captive breeding’– an emotionally loaded term later softened to ‘conservation breeding’– became a central justification for exhibiting animals to the public. The rationale was simple: animals kept in zoos and aquariums are ambassadors for their species and, through reproduction, can serve as an insurance against extinction in the wild. Of course, this idealized model (or ‘Noah's Ark paradigm’) relies on animals being genuinely threatened in nature, and kept safe and healthy in zoos or aquariums. The animals need to be cared for under circumstances where successful reproduction is possible, with the associated excellent husbandry, population management, welfare and veterinary care. Success also depends on founder individuals being genetically and in other ways biologically representative of the species and reproducing in sufficient numbers to constitute a viable population, perhaps in some cases for many decades. This original conception of an Ark related more or less to mammals and birds, and amphibians were certainly not a conspicuous element.
In the early 1990s, the notion of cooperatively managing Arks for various taxa led to the development within the zoo community of ‘species survival plans (SSPs)’; for example, SSPs of the American Association of Zoos and Aquariums (AZA) and European Endangered Species Programmes of the European Association of Zoos and Aquaria (EAZA). In support of this, Taxon Advisory Groups (TAGs), studbooks and computerized methods for zoological documentation and analysis were organized, notably through the International Species Information System (ISIS). All these initiatives focused on maintenance and breeding programmes and only a few species of amphibians were managed and recorded: a deficiency currently being addressed through the new Zoological Information Management System (ISIS–ZIMS). To ensure the appropriate husbandry conditions and management protocols in zoos, there also had to be a sufficient knowledge of population biology and habitat viability in the wild, and of the potential for ‘extinction vortices’– an area where specialist expertise of the IUCN Conservation Breeding Specialist Group of the Species Survival Commission has come to the fore, including in the present amphibian context.
It is ironic that the Ark concept has derived from and hitherto been applied almost exclusively to the charismatic ‘megavertebrates’ because these large-bodied animals require more space and other resources for their management. Conversely, resources applied to the conservation of the sometimes less popular or unappealing small-bodied vertebrates, including the amphibians, may accomplish much more. As Chair of the AZA Amphibian TAG, Kevin Wright wrote in the Amphibian TAG Regional Collection Plan (Wright, 2000):
The summation of the 1999 space survey is that there is only enough space existing in AZA institutions to accommodate 10 taxa of amphibians at the management level of PMP or SSP. In these same institutions there is enough space allocated for mammals to accommodate at least 57 SSPs and the majority of these mammals have a body mass of more than 10 kg and significant space requirements. If each AZA institution allocated an additional 400 square foot building to amphibian management and provided keeper support for the facility, the number of taxa that could be managed at a PMP or SSP level would easily exceed 100 taxa. If AZA is to “Keep all the Pieces”, the theme of its 1996 annual conferences, then a wave of dedicated amphibian facilities must be built. Amphibians need dedicated space and should not be simply incorporated into Reptile Houses or included as a small part of biome or zoogeographically-themed facilities. If this dedicated space is lacking, zoos will never play a major role in maintaining amphibian biodiversity.
In short, because of minimal space and other easily provided small-scale requirements, amphibians are ideal candidates for the Ark model – making it possible for zoos to save many species from extinction using only modest resources.
The logical extension of the original, generalized Ark model for all vertebrates was for zoos and aquariums or consortia to introduce zoo-bred animals back to nature to supplement or replace the threatened or extinct wild population, where the original causes for the decline were reduced or absent. Indeed, the Convention on Biological Diversity (CBD, 1992; and numerous publications of the IUCN/SSC Re-introduction Specialist Group) provides specific provision and encouragement for such reintroductions, when conditions are appropriate. The costs of all of this conservation work would mainly be borne by the money paid by visitors to see the animals, or through special fundraising.
Nonetheless, critics of conservation breeding and reintroduction maintain that these techniques can make only a minor contribution to the survival of species in the wild and that any claims to the contrary are exaggerated. There has, for example, been recent fierce debate over the declining genetic fitness of zoo populations bred over several generations with a view to reintroduction (Araki et al., 2007; Frankham, 2007; Hutchings & Fraser, 2007). Also Pounds et al. (2007) have expressed reservations about the utility of breeding in zoos and favour field-oriented conservation programmes for amphibians. This is despite ubiquitous global threats, a lack of reserve areas and the fact that even pristine and protected natural environments may contain rapidly declining populations of chytrid-infected frogs. Some more generalized arguments that may be advanced against SSPs operated ex situ by global, regional and national associations of zoos and aquariums is that these SSPs can become dissociated from conservation in situ and be mired in problems relating to data gathering and studbook analyses, population demographics, long-term genetic management, husbandry, veterinary care, quarantine, disposals, international transportation, space allocation, ownership, cooperative breeding agreements and even problems in ascertaining the precise taxonomic identity and provenance of livestock.
It is certainly true that there are still comparatively few direct links between ex situ zoo animal-management and breeding activities and in situ reintroduction or supplementation programmes, which follow guidelines of the IUCN/SSC Re-introduction Specialist Group. The success of these initiatives is so far only very limited and generally restricted to the more charismatic representatives of mammals and birds. However, zoos and aquariums can demonstrate some worthwhile and high-profile success in operating this model (Stanley Price & Soorae, 2003). While most reintroductions have been for higher vertebrates, there are now several for amphibians (Pavajeau, 2005; Zippel, 2005; Banks et al., in press). Indeed, amphibians are even considered by some as ideal candidates for such programmes (NCC, 1983; Corbett, 1989; Wiese & Hutchins, 1994; Bloxam & Tonge, 1995; Marsh & Trenham, 2001; Trenham & Marsh, 2002). For example, about 25% of wild Mallorcan midwife toads Alytes muletensis are the product of a successful zoo breeding and reintroduction scheme established by the Jersey Wildlife Preservation Trust (Q. Bloxam, pers. comm.). Techniques of assisted reproduction and cryopreservation have also been used to good effect in reintroduction programmes, as in the case of the Wyoming toad Bufo baxteri and Puerto Rican crested toad Bufo lemur SSPs. Nonetheless, critics also allege that in developing reintroduction programmes, the economic, social and educational needs of local people in the habitat countries who are dependent on (or in conflict with) wildlife are largely ignored (see Dodd & Seigel, 1991; Seigel & Dodd, 2002; for specific critiques of amphibian reintroduction programmes). Whatever the validity, or not, of such criticisms – and the zoo community must face them honestly and positively – they do not constitute a reason for zoos and aquariums to abandon their collective ideals or fail to rise to the challenges, however immense and daunting these may be, as in the case of the amphibian extinction crisis.
Building a Future for Wildlife: The World Zoo and Aquarium Conservation Strategy (WZACS, 2005) of the World Association of Zoos and Aquariums lights a new kind of beacon for conservationists to follow. The WZACS charts a course through all the foregoing complexities and bridges the gap between conservation activities in nature (in situ) and work in zoos and aquariums (ex situ) and demonstrates a potential for fully integrated and sophisticated approaches that are truly complementary. In the case of amphibians, it is now clear that veterinary treatment, population maintenance and conservation breeding ex situ (and subsequent re-introduction when the time is right) represent the only realistic hope for the existence of many species well into the 21st century. Also, the educational, communication and training roles of zoos, aquariums, botanical gardens and museums with living collections are potentially very powerful (Reid, 2007). With an estimated 600 million zoo visitors each year globally, no other community has the opportunity and potential to deliver conservation messages about frogs on such a direct and grand scale.
As one of only five major evolutionary units of the vertebrates, it is imperative that the integrity of this large, diverse and species-rich taxon is maintained. According to the IUCN Global Amphibian Assessment (Stuart et al., 2004) and supplementary data, there are in the order of 6000 valid species of amphibian; and (relying on other sources) there may be as many as 9000, if we include species that have not so far been scientifically described and the current rate of description. From this total, there are about 2000 threatened species, of which 442 are Critically Endangered and at least 500 immediately are in need of help through ex situ conservation programmes. The probable causes of the decline are multi-factorial, involving in various combinations the familiar issues of habitat destruction, fragmentation or loss, pollution (industrial, agricultural and pharmaceutical), over-harvesting, invasive species, disease and possibly the growing ecological impacts of climate change (Araújo et al., 2006; Alford et al., 2007; Rosa et al., 2007). In the latter case, it is known, for example, that the absence of rain for about 5–7 days in previously dense and continuously wet forests of Sri Lanka (now impacted by clearance for tea plantations) results in 100% reproductive mortality in foam-nesting (rhacophorid) frogs (Church, in press). Habitat loss evidently remains the most significant threat overall (impacting 90% of those species currently considered threatened). However, disease in the form of a chytrid fungus Batrachochytrium dendrobatidis is now the factor most commonly associated with enigmatic declines and catastrophic extinctions of amphibian populations and species (see Pessier, in press).
This chytrid fungus was first recognized in 1938 in the African clawed frog Xenopus laevis, which is believed to be largely resistant to its effects. Since the 1930s, this frog has been used in laboratories worldwide for experimental purposes and in testing for human pregnancies. With the discontinuation of this form of testing, these frogs may have been released everywhere by well-meaning laboratory staff or may have escaped accidentally, or the pathogens themselves have been carried in waste water. Apparently, by such means, the fungus has spread everywhere to indigenous species that had little or no resistance, and for which the chytrid infection could be lethal but recent work on a curative pharmaceutical treatment may confer some resistance (Poulter et al., unpubl.). However, this ‘out of Africa’ hypothesis remains to be tested thoroughly. In any event, the burgeoning global pet and food trade in live amphibians has likely facilitated the transmission of the disease and the infective fungus now exists in a sexually reproducing as well as vegetative form, which probably increases the potential for dispersal. Whatever the case, some 165 amphibian extinctions have been recorded from 1980 to date and, while many are likely to involve chytrid infections, the fundamental research still needs to be carried out. Chytridiomycosis is now well established and spreading in all amphibian-inhabited continents and can be characterized as ‘the worst infectious disease ever recorded among vertebrates in terms of the number of species impacted, and its propensity to drive them to extinction’ (IUCN, 2005).
This bleak situation prompted the calling by biologists and conservationists of an Amphibian Conservation Summit in September 2005, which has led to the production of a global Amphibian Conservation Action Plan or ACAP (published by IUCN/SSC: see Moore & Church, in press). To manage the ex situ aspects of the ACAP, an Amphibian Ark was formed (Pavajeau et al., in press). Today, with overwhelming threats of mass extinction, the ‘do nothing option’ or focusing only on preservation of habitats simply cannot be regarded as constructive alternatives. The amphibians are certainly a major case in point for a contemporary ‘Ark approach’ and the present account is dedicated to their survival.